Current Status of Phytoseiid Mites as Biological Control Agents in Latin America and Experiences from Argentina Using Neoseiulus californicus

Phytoseiidae is a large family of Mesostigmata mites. Members of this family are important biological control agents across the world since they are well-known natural enemies of phytophagous arthropods on cultivated and non-cultivated plants, mainly used to control pest spider mites. However, some can control thrips in greenhouses and fields. Several studies reporting on species in Latin America have been published. The most extensive studies were conducted in Brazil. Phytoseiid mites have been used in different biological control approaches, with two successful classical biological control programs: the biocontrol of the cassava green mite using Typhlodromalus aripo (Deleon) in Africa and the citrus and avocado mites by Euseius stipulatus (Athias-Henriot) in California. Efforts in using phytoseiid mites to enforce biological control of different phytophagous mites are being made in Latin America. Till now, only a few successful examples are available on this topic. This fact highlights the need to continue the investigations on the ability of other unknown species to be used in biological control through close collaboration between researchers and biocontrol companies. Various challenges remain, such as developing better rearing systems to provide a large number of predators to farmers in various crop systems, training farmers to improve their understanding of the use of predators, and chemical control aimed at conservation biological control, looking forward to increasing the use of the phytoseiid mites as biological control agents in Latin America and the Caribbean.


Introduction: an overview of the Phytoseiidae
Phytoseiidae is a large family of Mesostigmata mites, in which the number of species is being continuously revised.A total of 1500 species in 79 genera had been recognized in 1986, but these have increased to about 2300 species in 84 genera in 2007, while in 2012, 2692 species names were mentioned (including synonyms) (Demite et al. 2014(Demite et al. , 2022)).
Due to their predatory habits of feeding, Phytoseiid mites are important biological control agents all over the world since they are well-known natural enemies of phytophagous arthropods on cultivated and non-cultivated plants; mostly used to control pest spider mites, but some can control thrips and whiteflies in greenhouses and fields (Fathipour and Maleknia 2016).Although several other predatory mites are noted to control phytophagous mites, Phytoseiid mites have several advantages because of their high fecundity, abundant availability, good searching ability, dispersal rate, adaptability to different ecological niches, and a high degree of prey specificity (Gulati 2014).Besides, certain Phytoseiids consume large numbers of prey, maintain plant-feeding mites at low densities, and also have a rapid developmental rate comparable to their prey.Also, a female-biased sex ratio equivalent to their prey allows them to respond numerically to increased prey density, and can easily be mass-reared (Fathipour and Maleknia 2016).
Based on the diverse food sources used by Phytoseiid, McMurtry et al. (2013) proposed the new classification considering four lifestyles as follows: specialized mite predators (type I lifestyle), selective predators of tetranychid mites (type II lifestyle), generalist predators (type III lifestyle), and pollen feeding generalist predators (type IV lifestyle).Accordingly, Liu et al. (2017) showed a relationship between feeding habits and/or lifestyles of Phytoseiid based on variations in gnathostome morphology in which species are divided into three groups.Species in group II have larger chelicerae and hypostomes than those of groups I and III, while species in group III have larger lobes and angles of fixed digits than those of the other two groups.Although results were consistent with the previous classification, except that types I and II were not separated, authors indicated that feeding habits and lifestyles of Phytoseiids are also affected, apart from gnathostome morphology, by nutritional requirements, and digestive ability.It is necessary to evaluate the reliability of the method used by them and to discuss the possibilities for sub-grouping.
Based on the biological potential of Phytoseiid mites, and also due to the increasing requirements for alternatives to chemical control worldwide, more detailed studies should be addressed to investigate a large number of biological control candidates among this predatory mite family, mainly in Latin American countries where pest control is still based on chemical control.

The biodiversity of Phytoseiid mites in Latin America
Mites of the family Phytoseiidae (Mesostigmata) have been extensively studied for their potential as biological control agents of phytophagous mites (McMurtry and Croft 1997).
Conversely, a lower number of species have been reported in the different countries of Latin America (Fig. 1).
In Cuba, one of the first reports of Phytoseiidae mites was carried out by Smith and Summer (1949), who identified Phytoseiulus macropilis (Banks).Later, different studies have been done by Ramos and Rodríguez (2006), who provided the first list of this family in agroecosystems of Cuba, including new records (Table 2).de la Torre and Cuervo (2019) updated the list of Cuban mites, including 12 phytoseiid mites, but the crop or associated prey species were not stated (Table 2) by the author.
Regarding other Latin American countries, in Venezuela, the most remarkable study was made by Aponte and McMurtry (1993) who reported 31 species of phytoseiid mites found in several areas of the country, of which 19 species had not been reported for Latin America (Table 3).Other contribution related to a characterization of the acarofauna associated with Psidium guajava reported to Amblyseius tamatavensis, Euseius naindaimei, Proprioseiopsis ovatus, Neoseiulus caobae, and Typhlodromus paraevectus, as the new records for P. guajava (Quirós et al. 2005).
Similarly, the first studies in Colombia were made by Denmark and Muma (1972) who reported 11 species, describing two new species (Iphiseiodes zuluagai Denmark and Muma, on Citrus sp., and Passiflora edulis and Typhlodromips sinensis Denmark and Muma, on Citrus sinensis L.).In a second report of the phytoseiids of Colombia, Moraes et al. (1982) described a new genus and species, Quadromalus colombiensis and Euseius ricinus n. sp., bringing a total of 17 species to this country.Later, the number of species increased to 36, mainly belonging to Amblyseius (20 spp.), followed by Euseius (6 spp.), and Typhlodromus (5 spp.) (Moraes and Mesa 1988).Other less diverse genera included Phytoseius (2 spp.), Cydnodromella (1 sp.), Paraphytoseius (1 sp.), and Typhloseiopsis (1 sp.) with the description of three new species (Amblyseius bellottii from Banisteria sp., Amblyseius caliensis from Miconia sp., and Typhloseiopsis neopritchardi from Capsicum frutescens).The preponderance of Amblyseius species in Colombia was confirmed in a review made by Valencia et al. (2022) who contributed a list of main host plants to Phytoseiidae in Colombia (Table 3).
In other Caribbean islands, few are still known in most of the region.In the Dominican Republic, Ferragut et al. (2011) surveyed areas of natural vegetation and they reported 23 species, with Phytoseius dominicensis (Ferragut & Moraes) and Typhloseiopsis adventitius (Ferragut & Moraes) being described as the new taxa to science.In Puerto Rico, Denmark and Muma (1975) listed 48 species, including three new species named Typhlodromips plumosus, Typhlodromalus higuilloae, and Amblydromella deleoni.A more discrete number of species have been recorded in other Caribbean islands such as Belize (3 spp.), Antigua (2 spp.), Barbados, Bermuda, Haiti, and Saint Kitts with one species each (Demite et al. 2014).

Biological control of Phytophagous mites in Latin America: a brief comparison to other successful cases around the world
Phytoseiid mites have been used in different biological control approaches.In classical biological control programs, there are two long-term and successful projects based on the use of these predatory mites: the cassava green mite in Africa and the citrus and avocado mites in California.In the case of the cassava green mite, Mononychellus tanajoa, several phytoseiid species were introduced and released in Africa; however, only Amblydromalus manihoti (Moraes) and Typhlodromalus aripo De Leon were set (McMurtry et al. 2015).According to these authors, T. aripo showed a higher potentiality for pest control due to the high dispersal and consumption rates, and ability to persist in cassava fields, provoking a reduction of the pest population, which produced direct economic benefits of US$1.7, 74, and 384 billion for Nigeria, Benin, and Ghana, respectively (McMurtry et al. 2015).
Experiences in biological control of tetranychid mites in citrus and avocado in California reported more than 25 re-introduced and released species; however, only Euseius stipulatus has spread extensively from release sites four decades after releases (McMurtry et al. 2015).Consequently, E. stipulatus was introduced to and currently produced commercially in Peru in 2006 for the control of the citrus red mite.
A comparative study to evaluate the efficiency of two Amblyseius largoensis populations (La Réunion and the state of Roraima, Brazil) in controlling the invasive tenuipalpid mite, Raoiella indica, was carried out in Brazil; however, none of the populations exhibited efficacy to control the pest (Morais et al. 2016).These findings suggested the necessity of complementary studies under conditions as close as possible to those of natural fields to imitate the natural environment for fully grown plants and to increase the predation rate.Although A. largoensis is a promissory biological control agent for combating R. indica, this predator has not yet been commercially available, hence, the potential of Neoseiulus barkeri Hughes, a predator commercially available in Brazil, was evaluated against R. indica.Thus, the higher consumption and reproduction rates of N. barkeri fed on R. indica suggested N. barkeri is an effective predator to control the red palm mite as part of a biological control program (Filgueiras et al. 2020a, b).Moreover, according to Filgueiras et al. (2020c), this predatory mite showed a preference for eggs over other stages of the prey, which fitted a type II functional response.Accordingly, the higher the prey density, the higher number of eggs laid by N. barkeri females, but it tended to stabilize when the number of R. indica was greater than 80, suggesting that N. barkeri shows to be promissory in control R. indica populations.However, further studies are needed.
Concerning conservation biological control, generalist predatory mite species naturally occurring in agroecosystems, both on crops and adjacent natural vegetation, can be used to manage phytophagous mite populations.Tixier (2018) took some examples from three species, Kampimodromus aberrans, Euseius stipulatus, and Typhlodromus (Typhlodromus) pyri in vine and citrus crops, and the main lesson learned is that the occurrence database can help in determining the probability of finding predatory mite species on crops and non-crop plants.
Laboratory experiments carried out in Rio Grande do Sul, Brazil, demonstrated that Neoseiulus idaeus (Denmark & Muma) completed its development when feeding on Mononychellus planki (McGregor), Tetranychus ludeni (Zacher), and Tetranychus urticae (Koch), suggesting that this predator mite may be utilized in biological control; however, further studies are required to define predator's performance in the field (Reichert et al. 2017).Additionally, since N. idaeus is commonly found in semiarid regions of South America, laboratory assays compare the predation and oviposition rates of a drought-tolerant strain with the performance of a commercial species, Neoseiulus californicus (McGregor) (Sousa-Neto et al. 2021).Drought-tolerant N. idaeus showed a higher predation rate and similar oviposition performance as compared to N. californicus, and in addition, N. idaeus showed a higher searching rate even at low prey density on cowpea, suggesting that N. idaeus is a good candidate to control T. urticae, especially in semiarid regions.
Experiences in using phytoseiid mites to control pests other than mites have also been reported.Cavalcante et al. (2017) evaluated the potential of a Brazilian population of Amblyseius tamatavensis to manage Bemicia tabaci populations on artificially infested bell pepper (Capsicum annuum L) plants under laboratory conditions (28 ± 1 °C, 80 ± 10% RH, and 12 h of daily photoperiod).When released on artificially infested bell pepper plants, A. tamatavensis completed immature development in 5.1 days with an oviposition mean rate of 1.0 eggs/female/day, reducing the population density of B. tabaci by 60 to 80%, indicating that this phytoseiid mite is a promising biological control agent of B. tabaci biotype B.
Efforts in using phytoseiid mites to implement biological control of different phytophagous mites are being made in Latin America; however, more detailed laboratory and field studies are required to improve our knowledge about rearing and release techniques, habitat management strategies, susceptibility to agrochemicals, predation efficiency, interaction with other organisms of the agroecosystem, among others.

Current status of predatory mites as biological control agents in Latin America
Predatory mites, mainly from the family Phytoseiidae (Acari: Mesostigmata), are used to control mite pests, as well as small insects throughout the world.The Phytoseiidae family contains more than 2692 species and the countries with the highest number of reported species are the USA, China, India, Brazil, and Pakistan (Demite et al. 2022).Some of these species are used as agents by all three widely recognized biological control strategies: (1) classical biological control to control, invasive pests introducing them in the targeted area, from the pest origin region (De Clercq et al. 2011); (2) augmentative biological control that consists of a mass release of the exotic or endemic, biological control agent in crops (van Lenteren 2012(van Lenteren , 2017)); and (3) conservation biological control that consists of enhancing the performance of natural enemies in the crops through the agroecosystem management (Tixier 2018).
Around 38 species of predatory mites are commercially produced in the world, representing 13% of all arthropods used (van Lenteren et al. 2017).The mites most used as the control agents are Phytoseiulus persimilis (Athias-Henriot) (type I lifestyle) and Neoseiulus californicus (McGregor) (type II lifestyle) for the control of the two-spotted spider mite Tetranychus urticae (Koch), and Amblyseius swirskii Athias-Henriot (type III lifestyle) for control of thrips and whiteflies in greenhouses.In Latin America, 10 species of Phytoseiidae have been used in different countries, from their region of origin or another, through classic biological control programs and, sometimes, in combination with augmentative biological control (Table 4).Several species (about 14), exotic and native, are used by this last strategy (van Lenteren et al. 2020).Most predatory mites are food-generalists, which can feed on many prey and plant exudates, pollen, and fungi, and they are naturally present both on crops and on adjacent natural vegetation.Such characteristics make them good candidates for conservation biological control implementation, so several studies have advanced in this sense, describing the relationship of Phytoseiid with the natural vegetation surrounding crops (Tixier 2018).

Experiences with Neoseiulus californicus in Argentina
Neoseiulus californicus is distributed in Europe, Japan, South Africa Canada, North America, and South America (Demite et al. 2022) and is used by augmentative releases in numerous countries, such as the Netherlands, Belgium, Spain, Israel, Japan, USA, Mexico, Brazil, Colombia, and Chile where it is massively raised and marketed.
Members of type II of the Phytoseiidae family have a preference for a broad range of tetranychid species, but they also feed and reproduce on mites of other groups, including Eriophyidae, Tarsonemidae, and Tydeoidea, and also on pollen (McMurtry et al. 2013;Khanamani et al. 2017;Soltaniyan et al. 2018Soltaniyan et al. , 2020)).Commercial Typha angustifolia pollen Nutrimite® is an acceptable food for N. californicus because it enables this predator to develop and reach adulthood, as well as reproduce and have viable offspring, although their performance is significantly higher when it feeds on T. urticae (Pascua et al. 2020).
Strains from different geographic areas often differ in some population parameters and tolerance or susceptibility to certain factors, such as drought, insecticides, and winter conditions.In Argentina, there are no biofactories that produce this control agent, but several studies that have been carried out on its ecology suggest that it is possible to implement conservation biological control strategies, particularly in strawberry crops in the horticultural belt of La Plata, Buenos Aires (34°56′00″S, 57°57′00″W).In strawberry greenhouses, Greco et al. (1999) found both T. urticae and N. californicus populations were widely distributed, although, in general terms, N. californicus exhibited an uneven aggregation than T. urticae.This would create refugees for the prey, thus increasing the persistence of the system.The high spatial coincidence of N. californicus with T. urticae indicates an important dispersal capacity of the predator, and a high ability to detect leaflets with prey (Greco et al. 2005).
Several wild plants surrounding crops may provide temporary habitat and potential food sources for N. californicus californicus when the strawberry crop is ending and offers scarce food resources.Although the pollen of these plants would not enable the predator population to increase, the presence of these plants in the vicinity of strawberries could contribute to the persistence of the N. californicus population and help to limit T. urticae growth when this pest begins to colonize the crop (Gugole Ottaviano et al. 2015).
The ability to resist winter conditions and periods of starvation is another characteristic of this strain.Greco et al. (2006) found a survival of 62.5% after 96 h of starvation, and it has recently been observed that females can survive 10 days without food (Alonso, personal communication).Although total fecundity decreased due to a reproductive diapause during starvation, the number of offspring produced by females after the periods of starvation was not significantly different from those fed females, they leveled at approximately 2.9 eggs per female per day.Besides, the fecundity of individuals of this N. californicus strain decreased significantly under winter conditions, but reproductive diapause might not be observed.In the laboratory, individuals exposed to winter conditions throughout the life cycle exhibited a long pre-oviposition period, and low oviposition rate but did not diapause.After being kept under winter conditions from larva to adult, when individuals were transferred to the optimal spring temperatures and lighting, the pre-oviposition period was shorter, and the fecundity was higher than under winter conditions.When it remained under spring conditions from larva to adult and was then transferred to the winter parameters during the first 15 days of adulthood, the pre-oviposition period was long and the oviposition rate was low.Once the optimal conditions were restored, the daily fecundity became similar to that of the individuals remaining under optimal conditions throughout the life cycle (Gugole Ottaviano et al. 2018).
All these features suggest that N. californicus is a good candidate for conservation biological control in La Plata, Buenos Aires.A management plan for T. urticae in strawberries, based on the natural control by N. californicus, and acaricide applications only when necessary was developed and validated (Greco et al. 2011).The plan has two components: a sampling protocol and a decision chart.Systematic presence-absence sampling of active T. urticae and N. californicus was used to predict prey and predator densities relying only on the proportion of T. urticae-infested leaflets, once the occurrence of the predator was detected in at least one of them (Greco et al. 2004).The decision chart was constructed taking into account the relative pest and predator densities and the pest's rate of increase (Greco et al. 2005).It determines the range in the proportion of T. urticae-infested leaflets that will require different actions: to use selective acaricides and re-check at 7 days, to take no action but re-check at 7 days, and to take no action but re-check at 14 days.The management plan is potentially effective and feasible, showing that natural populations of N. californicus can consistently produce strong top-down suppression of T. urticae.It was experimentally implemented in 11 commercial lots for 2 years, and it was found that spider mite densities remained low and similar to those of lots under conventional management.The management plan's application reduced the usage of acaricides by 90% and needs much less time (25% less) than applying acaricide in an area of the same size (Greco et al. 2011).This biological conservation method, which reduces the frequency of acaricide usage to conserve the predator, might be supplemented by occasional augmentative releases, as shown by the same proposal to abolish chemical control for T. urticae in strawberries.
Other helpful knowledge for biological control through this agent in integrated management plans is the compatibility between this strategy and others, such as the use of resistant cultivars to T. urticae.Gugole Ottaviano et al. (2013) found that Festival and Albion could be suitable strawberry cultivars used in T. urticae management programs that include biological control by N. californicus.Ultimately, two other aspects are being investigated: (1) dispersal based on resource availability and (2) intraguild predation by Orius insidiosus Say (Hemiptera: Anthocoridae), the main predator of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae); to determine the compatibility of these agents for the control of two crucial strawberry pests.

Final remarks
Biological control using leaf-inhabiting phytoseiid has been booming during the last decades, since these predatory mites play a significant role in the biological control of mites and insect pests.Therefore, they have been the subject of intensive studies across the world, including several Latin American countries, mainly Brazil and México.These studies have resulted in an important number of new species described, as well as a wide knowledge of bioecology, geographic distribution, predation capacity, etc.Nevertheless, till now, few species are effectively used in biological control programs.
This fact highlights the need to continue the investigations on the ability of other, unknown species to be used in biological control through close collaboration between researchers and biocontrol companies.Still, different challenges such as developing better rearing systems to provide huge numbers of predators to farmers in different crop systems, training farmers to improve their understanding of the use of predators, and chemical control aiming to reinforce the use of conservation biological control.

Table 3
The main species of Phytoseiidae reported according to plant species in Colombia

Table 4
Phytoseiidae used by classic biological control (CBC) and/or augmentative biological control (ABC) projects in Latin America a Entered as Amblyseius chilensis(Crouzel 1983)and reintroduced in 2007 Lamium amplexicaule L., Convolvulus arvensis L., Sonchus oleraceous L., Galega officinalis L., allowed the development of N. californicus adult, but not a reproduction.Survival was 70-80% when fed on pollen from S. oleraceus, G. officinalis, and C. arvensis, 80-90% when fed on pollen from U. urens and F. x ananassa, and more than 90% when fed on T. urticae and pollen from L. amplexicaule.In autumn and winter, U. urens, L. amplexicaule, and S. oleraceous could promote the persistence of N. californicus when prey density in strawberry is low since this plant species provide supplementary food sources.In summer, pollen of C. arvensis and G. officinalis would contribute to the persistence of N.